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Morphology and Life History Divergence in Cave and Surface Populations of Gammarus Lacustris (L.)

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Morphology and Life History Divergence in Cave and Surface Populations of Gammarus Lacustris (L.) RESEARCH ARTICLE Morphology and life history divergence in cave and surface populations of Gammarus lacustris (L.) 1,2 2² 3 4 Kjartan ØstbyeID *, Eivind Østbye , Anne May Lien , Laura R. Lee , Stein- Erik Lauritzen5, David B. Carlini6 1 Inland Norway University of Applied Sciences, Department of Forestry and Wildlife Management, Campus Evenstad, Koppang, Norway, 2 Center for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway, 3 Knut Bjørhuus vei 35 C, Drammen, Norway, 4 Department of Biology, Stanford University, Stanford, CA, United States of America, 5 Department of Earth Science, University of Bergen, Allegaten 41, Bergen, Norway, 6 Department of Biology, American University, a1111111111 Washington, D.C., United States of America a1111111111 ² Deceased. a1111111111 * [email protected] a1111111111 a1111111111 Abstract Cave animals provide a unique opportunity to study contrasts in phenotype and life history OPEN ACCESS in strikingly different environments when compared to surface populations, potentially Citation: Østbye K, Østbye E, Lien AM, Lee LR, related to natural selection. As such, we compared a permanent cave-living Gammarus Lauritzen S-E, Carlini DB (2018) Morphology and lacustris (L.) population with two lake-resident surface populations analyzing morphology life history divergence in cave and surface (eye- and antennal characters) and life-history (size at maturity, fecundity and egg-size). A populations of Gammarus lacustris (L.). PLoS ONE part of the cytochrome c oxidase subunit I gene in the mitochondrion (COI) was analyzed to 13(10): e0205556. https://doi.org/10.1371/journal. pone.0205556 contrast genetic relationship of populations and was compared to sequences in GenBank to assess phylogeography and colonization scenarios. In the cave, a longer life cycle was Editor: Sylvie ReÂtaux, Centre National de la Recherche Scientifique, FRANCE implied, while surface populations seemed to have a shorter life cycle. Egg size, and size at maturity for both sexes, were larger in the cave than in surface populations, while fecundity Received: October 12, 2017 was lower in the cave than in surface populations. The cave population had longer first- and Accepted: September 27, 2018 second antennae with more articles, longer first- and second peduncles, and fewer omma- Published: October 25, 2018 tidia than surface populations. The cold low-productive cave environment may facilitate dif- Copyright: © 2018 Østbye et al. This is an open ferent phenotypic and life-history traits than in the warmer and more productive surface lake access article distributed under the terms of the environments. The trait divergences among cave and surface populations resembles other Creative Commons Attribution License, which cave-surface organism comparisons and may support a hypothesis of selection on sensory permits unrestricted use, distribution, and reproduction in any medium, provided the original traits. The cave and Lake Ulvenvann populations grouped together with a sequence from author and source are credited. Slovenia (comprising one genetic cluster), while Lake Lille Lauarvann grouped with a Data Availability Statement: All data are available sequence from Ukraine (comprising another cluster), which are already recognized phyloge- as supplementary information. netic clusters. One evolutionary scenario is that the cave and surface populations were colo- Funding: Funded by Inland Norway University to nized postglacially around 9 000±10 000 years ago. We evaluate that an alternative Mr. Kjartan Østbye. The funders had no role in scenario is that the cave was colonized during an interstadial during the last glaciation or study design, data collection and analysis, decision earlier during the warm period before onset of the last glaciation. to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. PLOS ONE | https://doi.org/10.1371/journal.pone.0205556 October 25, 2018 1 / 32 Morphology and life history in cave and surface populations of Gammarus lacustris Introduction Caves represent evolutionary model systems to study trait changes in the cave living fauna as compared to their relatives on the surface [1±3]. Striking apparent adaptations in morphology and life-history in cave animals have intrigued scientists for centuries [4±6]. Such cave dwell- ing populations, or species, often display trait reductions (often termed regressive evolution), reduced sight or even the complete loss of eyes and pigmentation, but attenuation of other appendages, as well as enhancement of extra-optic sensory structures, when compared to rela- tives outside the cave environment [7,8]. Since most obligate cave species (i.e. permanent resi- dents of caves) often lack extant surface populations, or close taxonomic relatives, being separated for extended evolutionary time, they may not constitute the most ideal study objects for assessment of the very early stages of cave associated trait shifts and evolutionary changes. Facultative cave species (i.e. that also occupy surface areas) may better represent early stages in evolution of cave associated trait alterations where gene flow with surface populations still occurs or have recently been terminated [9±11]. The frequently observed infertility between cave and surface populations may also provide a possibility to analyze the genetic basis of com- plex traits [12,13]. Thus, cave animals are excellent model systems for studying speciation mechanisms at different stages in a long process [3,14±16]. Several hypotheses have been issued to test apparent evolution of trait divergence between cave and surface populations as seen in many organisms [7,17±19]. First, natural selection may reduce the economy allocated to an unused structure such as eyes in a dark and nutrient poor environment in caves to reallocate energy to more important traits. Alternatively, trait changes in surface and cave populations may be due to random genetic drift affecting evolutionary selected, neutral- or nearly neutral traits in small founder populations. Thus, trait changes may stem from different scenarios; (i) genetic drift on traits that are selected, neutral or nearly neu- tral in adaptation, (ii) single adaptive traits exposed to natural selection, (iii) correlated natural selection through simultaneous selection on two or more genetically independent traits, (iv) pleiotropy with selection on one single trait while other traits are tagging along due to genetic hitch-hiking and genomic linkage, or (v) a combination of these mechanisms, or other alterna- tive phenotype-genotype mechanisms through gene expression pathways [6,12,20,21]. Here, phenotypic plasticity and epigenetics may also be important mechanisms in trait divergence in surface and cave environments, but have not yet been explored in much detail. At any rate, the apparent general similar selective pressures in caves seem to a large extent to result in remark- ably similar evolutionary solutions to shared environmental challenges even for distantly related taxa [3,8,22]. In North America, the amphipod Gammarus minus has repeatedly colonized independent limestone caves from ancestral surface lake systems [19]. Here, traits usually do not differ between cave-dwelling and surface populations except for cave populations located in the Greenbrier Valley karst of West Virginia and in Tazewell County, Virginia. In these regions, cave populations are often highly modified phenotypically, have reduced eyes, fewer omma- tidia, larger body size, longer antennae, and reduced pigmentation. Such morphological differ- ences are attributed to natural selection [19,20,23,24], where genetic studies show that populations cluster based on hydrology rather than based on cave or surface environments [25]. Thus, for G. minus, troglomorphic characters have evolved independently in parallel due to repeated colonization of individuals of the surface populations dwelling at the spring where the cave water resurges [9]. Strong support for natural selection as a driver in phenotypic dif- ferences is observed in collapsed caves with G. minus, which then opens up a surface environ- ment to the cave adapted populations, where subsequently natural selection towards functional eye structures evolves [19]. In a laboratory study, Fong [20] observed negative PLOS ONE | https://doi.org/10.1371/journal.pone.0205556 October 25, 2018 2 / 32 Morphology and life history in cave and surface populations of Gammarus lacustris pleiotropy for reduction or loss of eye structures and increased antennae structures in cave-liv- ing G. minus, suggesting that one or both traits may be targeted by selection, while no negative pleiotropy was found within or between the surface populations of G. minus. Moreover, phylo- genetic and population genetic studies often suggest that populations of cave species have a small effective population size (Ne), lower genetic diversity, and reduced gene flow with their related surface populations [26±29]. Also, low genetic diversity and amino-acid codon usage bias may indicate bottlenecks, and further suggest constraint on adaptive evolution in cave population of G. minus [25]. A relative to the North American Gammarus minus is G. lacustris (G. O. Sars), which has a circumpolar distribution [30,31] from low altitude calcium-rich lakes to high altitude cold and often calcium-poor lakes [32]. The life-cycle in lowland areas are generally annual and semel- parous (life
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